Phylogenetic relationships of Malayan and Malagasy pygmy shrews of the genus Suncus (Soricomorpha: Soricidae) inferred from mitochondrial cytochrome B gene sequences

2011·0.51 MB·English

by  Omar, Hasmahzaiti

THE RAFFLES BULLETIN OF ZOOLOGY 2011
THE RAFFLES BULLETIN OF ZOOLOGY 2011 59(2): 237–243
Date of Publication: 31 Aug.2011
© National University of Singapore
PHYLOGENETIC RELATIONSHIPS OF MALAYAN AND MALAGASY PYGMY
SHREWS OF THE GENUS SUNCUS (SORICOMORPHA: SORICIDAE) INFERRED
FROM MITOCHONDRIAL CYTOCHROME B GENE SEQUENCES
Hasmahzaiti Omar
Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur
Email: [email protected] (Corresponding author)
Eleanor A. S. Adamson
Genetics and Molecular Biology, Centre for Research in Biotechnology for Agriculture,
Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur
Subha Bhassu
Genetics and Molecular Biology, Centre for Research in Biotechnology for Agriculture,
Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur
Steven M. Goodman
Department of Zoology, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA
Association Vahatra, BP 3972, Antananarivo (101), Madagascar
Voahangy Soarimalala
Association Vahatra, BP 3972, Antananarivo (101), Madagascar
Rosli Hashim
Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur
Manuel Ruedi
Department of Mammalogy and Ornithology, Natural History Museum of Geneva, 1208 Geneva, Switzerland
ABSTRACT. – This study used a portion of the mitochondrial cytochrome b gene to investigate the phylogenetic
relationships of Suncus pygmy shrews and to help clarify the taxonomic status of the Malayan pygmy
shrew (S. malayanus) and the Malagasy pygmy shrew (S. madagascariensis). Phylogenetic reconstructions
were performed using neighbour-joining and Bayesian analysis methods and revealed that S. malayanus is
related to, but distinct from S. etruscus. The K2P-corrected genetic distance among the Malaysian taxon
and other pygmy shrews for the cytochrome b gene was between 6.1 and 8.5%, supporting recognition that
S. malayanus represents a distinct species from the geographically widespread S. etruscus species complex.
A close (1.5% K2P distance) sister-group relationship was revealed between S. etruscus from Sri Lanka
and S. madagascariensis from Madagascar, which has been considered an island endemic, and suggests
that these animals are not specifi cally distinct. The Malagasy population of this shrew most probably was
translocated to the island by human intervention, with the lineage originating from Southeast Asia or the
Indian subcontinent.
KEY WORDS. – Crocidurinae, cytochrome b, genetic distance, mitochondrial DNA, phylogenetic relationships,
Suncus.
INTRODUCTION regarding species limits within the genus. For instance, S.
malayanus (Fig. 1), the principal focus of this study, was
Due to their extremely small size (about 2 g), pygmy shrews initially named Pachyura malayana by Kloss (1917) and
of the genus Suncus (Family Soricidae) are diffi cult to trap subsequently considered a subspecies of the Etruscan shrew S.
and are therefore poorly represented in reference collections, etruscus (Savi, 1822) under the name S. etruscus malayanus
which in turn has added to ongoing taxonomic confusion (see e.g. Medway, 1978). More generally, Ellerman &
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Omar et al.: Phylogenetic relationships of pygmy shrews
Morrison-Scott (1966) and Corbet & Hill (1992) considered, specimens were either prepared as fl at skins or fi xed in
with some reservation, that all pygmy shrews occurring in the 5% formalin and subsequently transferred to 70% ethanol.
Indomalayan region were part of a single widespread species, Kidney samples were removed soon after death and stored at
S. etruscus, originally described from specimens collected –80oC or preserved in 95% ethanol for genetic analysis. The
in Italy. Numerous authors, including recent overviews of voucher specimens are housed at the Zoological Department,
Southeast Asian mammals (Francis, 2008), adopted this view. University of Malaya. The specimens of S. madagascariensis
However, in his revision of the Soricidae, Hutterer (2005) were collected in the dry deciduous forest of Beanka, near
recognised four additional, geographically restricted species Maintirano (S18°03.75' E44°31.5'E, altitude 320 m) with the
in the etruscus group: S. fellowesgordoni (Phillips, 1932) use of pitfall traps. Muscle tissue samples from these animals
from the highlands of Sri Lanka, S. malayanus from the were preserved in EDTA. Other Suncus samples were also
Thai-Malay peninsula, S. hosei (Thomas, 1893) from Borneo employed in this study and the genus Myosorex was employed
and S. madagascariensis (Coquerel, 1848) from Madagascar. as the outgroup (see below and Table 1).
These various forms differ slightly in morphology from
European S. etruscus but live in very different habitats, and DNA extraction, PCR amplification and sequencing.
were considered endemic to their specifi c regions (Hutterer, – DNA was extracted from preserved tissue samples using
2005). Promega Wizard extraction kits following the manufacturer’s
protocol (Promega Co.). Polymerase chain reaction (PCR)
Molecular phylogenetic techniques have been employed amplifi cation of the target fragment of the mitochondrial
to clarify aspects of the systematic relationships among cytochrome b gene was performed using primers L14724
other groups within the family Soricidae and subfamily and H15915 (Irwin et al., 1991). 25 µl PCR reactions
Crocidurinae (e.g. Jenkins et al., 1998; Ruedi et al., 1998; contained 5 µl of DNA template (~20 ng/µl), 2.5 µl of
Motokawa et al., 2000; Quérouil et al., 2001; Ohdachi et al., each primer (10 mM), 0.5 µl of dNTP (10 mM), 2.0 µl of
2004; Dubey et al., 2007; Meegaskumbura & Schneider, 2008; MgCl of (25 mM), 2.5 µl of 5x colorless GoTaq ® Flexi
2
Meegaskumbura et al., 2010). These studies have shown that buffer and 0.2 µl of GoTaq DNA Polymerase (5 u/µl). PCR
within the Crocidurinae the genus Suncus is paraphyletic with conditions were as follows: 40 cycles of denaturation at 93oC
the genera Sylvisorex and Crocidura (Quérouil et al., 2001; for 45 s, annealing at 45.9oC for 45 s, extension at 72oC
Dubey et al., 2007), with Suncus etruscus basal to other Asian for 1 min, with a fi nal extension at 72oC for 5 min. PCR
Suncus and the remaining members of the Crocidurini tribe products were electrophoresed on a 1% agarose gel then
(Dubey et al., 2008). Large divergence among populations visualised with ethidium bromide staining to check success
of this genus formally classifi ed as a single taxon (e.g. S. of PCR amplifi cation. PCR products were gel purifi ed using
murinus; Meegaskumbura & Schneider, 2008), suggests Promega Wizard SV Gel and PCR Clean up System with
that additional cryptic taxonomic diversity exists. Although microcentrifudge (Promega Co.). Cleaned amplicons were
adding to systematic knowledge of the group, these studies sequenced in both directions using the same primers by a
have generally not addressed the relationships among certain commercial laboratory (First Base Co., Selangor, Malaysia)
Asian members of pygmy shrews including S. malayanus. using a BigDye ® Terminator v3.0 Cycle Sequencing Kit
with products run on an ABI 3730 automatic sequencer.
In this study, we present an analysis of mitochondrial DNA
sequence data to determine the phylogenetic relationships and Sequence alignment and phylogenetic analyses. – New
genetic distances between S. malayanus, S. madagascariensis sequence data from the cytochrome b gene of three S.
and S. etruscus. The results help to clarify their taxonomic malayanus from Malaysia, two S. madagascariensis from
status and document new occurrences of S. malayanus at Madagascar and one S. etruscus from France was obtained
three sites across the Thai-Malay peninsula, including one in the current study. The sequences were edited using
from a montane location. Chromas version 1.45 (MacCarthy, 1996). Another 13 Suncus
cytochrome b sequences, representing additional samples of
MATERIAL AND METHODS
Sample collection. – Samples of Suncus malayanus (Fig. 1),
were collected from three locations in Peninsular Malaysia:
Ulu Gombak (N03o60.170' E101o60.46', altitude 200 m),
Bukit Rengit [=Rengit Hill] (N03o35.987' E102o10.758',
altitude 132 m) and Cameron Highlands (N04o28.460'
E101o23.05', altitude 1465 m). These locations are covered by
extensive secondary lowland evergreen forests (Ulu Gombak
and Bukit Rengit) or by montane forests surrounding tea
plantations (Cameron Highlands). At each site shrews were
captured in 50–100 unbaited pitfall traps (buckets dug into
Fig. 1. Male Malayan pygmy shrew (Suncus malayanus) captured
earth) set within a 45 × 45 m grid. All individuals were
in the Cameron Highlands, Pahang, Peninsular Malaysia, in a pitfall
euthanized immediately after capture using chloroform.
trap set on the forest fl oor. Notice the characteristic large ears and
Sex and external measurements were recorded, and the
dark fi ne pelage.
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Table 1. List of all Suncus and Myosorex (outgroup) specimens that were used in this study with information on collection site, country
and GenBank accession number. The numbers given after the species names are associated with the sample numbers of the different taxa
and are used in Table 2.
Species Collection site Country GenBank Reference
(Locality) accession number
(cytochrome b)
Suncus malayanus1 Ulu Gombak (Selangor) Malaysia JF817391 This study
S. malayanus2 Cameron Highlands (Pahang) Malaysia JF817392 This study
S. malayanus3 Bukit Rengit (Pahang) Malaysia JF817393 This study
S. madagascariensis1 Beanka Forest Madagascar JF817394 This study
S. madagascariensis2 Beanka Forest Madagascar JF817395 This study
S. etruscus1 Anuradhapura Sri Lanka FJ716836 Meegaskumbura & Schneider (2008)
S. etruscus2 Fivizzano Italy DQ630397 Dubey et al. (2007)
S. etruscus3 Camargue France DQ630396 Dubey et al. (2007)
S. etruscus4 Gard France JF817396 This study
S. montanus1 Agarapathana Sri Lanka GQ290378 Meegaskumbura & Schneider (2008)
S. montanus2 Morningside Sri Lanka FJ716835 Meegaskumbura & Schneider (2008)
S. niger (previously Nilgiri Hills India DQ630388 Dubey et al. (2007)
analysed as montanus)
S. murinus1 Negros Island Philippine FJ813963 Esselstyn et al. (2009)
S. murinus2 – India EU122224 Meegaskumbura & Schneider (2008)
S. remyi Moueva Gabon DQ630399 Dubey et al. (2007)
S. dayi Nilgiri Hills India DQ630432 Dubey et al. (2007)
S. stoliczkanus1 – Nepal AB175077 Ohdachi et al. (2004)
S. stoliczkanus2 – Nepal AB175076 Ohdachi et al. (2004)
S. varilla – South Africa DQ630434 Dubey et al. (2007)
Myosorex cafer Serola South Africa FJ814024 Dubey et al. (2007)
M. sclateri Natal South Africa FJ814043 Dubey et al. (2007)
S. etruscus from France and Italy and a further six Suncus MrBayes version 3.0 (Huelsenbeck & Ronquist, 2001) with
species were compiled from GenBank records, along with one million generations implementing Metropolis-Coupled
cytochrome b sequences for two outgroup taxa, Myosorex Markov Chain Monte Carlo (MCMCMC) with trees sampled
cafer and M. sclateri (Table 1). The initial 270 base-pairs of every 1000 generations. Tree parameters reached stationary
the sequences of S. etruscus from Italy deposited by Dubey et distributions after a burn-in period of 100,000 generations.
al. (2007) under GenBank number DQ630397 were omitted Posterior probabilities (PP) were calculated for each node
because of unreliable readings. Multiple alignments of all as the percentage of sampled trees containing the node in
sequences were performed with ClustalX 1.81 (Thompson question.
et al., 1997). Missing nucleotides in partial sequences were
replaced by N in the fi nal alignment. Estimates of pairwise
genetic distance among cytochrome b gene fragments from RESULTS
the different forms of pygmy shrews were calculated using
the Kimura two-parameter (K2P) model (Kimura, 1980) We obtained between 1013 (from the three Malayan
implemented in MEGA 4 software (Tamura et al., 2007). samples) and 1140 base-pairs (from the single French and
two Malagasy samples) of the cytochrome b gene, which are
We conducted phylogenetic analyses to illustrate the level deposited in GenBank under numbers JF817391 – JF817396.
of divergence and relationships among all sampled taxa. All 21 sequences used in the phylogenetic reconstructions
Trees were constructed by using neighbour-joining (NJ) and distance calculations represented 10 putative Suncus
and Bayesian analysis (BA) methods. All trees were rooted and two Myosorex species (Table 1). The fi nal alignment
with Myosorex spp. as the outgroup. The NJ analysis was represented 704 conserved sites, and 366 of the 436 variable
conducted using MEGA 4 (Tamura et al., 2007) with the sites proved to be parsimony-informative. Corrected (K2P)
K2P distance matrix and uniform rates across sites. Bootstrap pairwise genetic distances among the pygmy Suncus are
analysis used 1000 replications to compute 50% majority shown in Table 2, with the African pygmy shrew, S. remyi,
rule consensus trees for node confi dence limits (Felstenstein, also included for comparison as a distant relative (Dubey
1985). For BA phylogenetic analysis, trees were constructed et al., 2008). They reveal relatively high inter-specific
using the TrN + I + G model of DNA evolution that best fi ts genetic distances (6.1–8.5%) between S. malayanus and S.
data according to the protocol of Posada & Crandall (1998) madagascariensis or S. etruscus, but much greater distances
implemented in Modeltest version 3.7. BA was performed in when compared to S. remyi (23.6–24.0%). Among the three
239
Omar et al.: Phylogenetic relationships of pygmy shrews
Table 2. Percent pairwise corrected (K2P) genetic distance among the pygmy shrews Suncus malayanus, S. madagascariensis, S. etruscus
and S. remyi cytochrome b sequences.
Sample 1 2 3 4 5 6 7 8 9
1 S. malayanus1 Malaysia –
2 S. malayanus2 Malaysia 1.4 –
3 S. malayanus3 Malaysia 0.3 1.1 –
4 S. madagascariensis1 Madagascar 8.0 8.5 7.7 –
5 S. madagascariensis2 Madagascar 8.0 8.5 7.7 0.1 –
6 S. etruscus1 Sri Lanka 7.6 8.0 7.3 1.5 1.4 –
7 S. etruscus2 Italy 6.6 6.9 6.1 3.3 3.3 3.4 –
8 S. etruscus3 France 6.9 7.3 6.4 3.1 3.1 3.3 0.4 –
9 S. etruscus4 France 7.1 7.6 6.8 3.1 3.0 3.6 0.3 0.1 –
10 S. remyi Gabon 24.0 23.9 23.6 23.5 23.5 23.3 21.7 21.1 21.8
S. malayanus sequenced, the two lowland individuals from complex (sensu Corbet & Hill, 1992) is also found at the
Bukit Rengit and Ulu Gombak were more closely related molecular level. Our results show that Eurasian S. etruscus
to each other (0.3% K2P divergence), than they were to are closely related genetically to S. madagascariensis, but
the individual from the Cameron Highlands (1.1 and 1.4% not to S. malayanus. Aside from the pygmy shrews, the other
divergence). Intra-specifi c divergences among S. etruscus relationships identifi ed herein among Suncus species are in
individuals collected in Europe were minimal (0.1–0.4% agreement with earlier fi ndings, such as close relationships
which corresponds to one to three point mutations), but between S. murinus and S. montanus (Meegaskumbura
higher (up to 3.6% or 39 point mutations) when the sample & Schneider, 2008), and the distinct position of S. niger
from Sri Lanka was included. This distance is comparable relative to other large Suncus (Meegaskumbura et al., 2010).
to the divergences measured between European samples In addition, the separation of the African and Eurasian taxa
of S. etruscus and S. madagascariensis (3.0–3.3%). The into two clades (Fig. 2A) mirrors the relationships observed
lowest inter-specifi c divergence (1.4–1.5%) was observed by Dubey et al. (2008) based on a more comprehensive
between the Sri Lankan S. etruscus and Malagasy S. taxonomic and larger character sampling of Crocidurinae
madagascariensis, identifying a close genetic distance shrews.
between these individuals.
Previous studies of divergence in the cytochrome b gene of
The phylogenetic trees constructed using the two methods mammals in general (Bradley & Baker, 2001) or Crocidurinae
(NJ and BA) were largely congruent (Fig. 2). Both analyses in particular (Ohdachi et al., 2004; Dubey et al., 2006) have
identifi ed a major clade among Suncus corresponding to all found that divergences of between 1.5 and 2.4% indicate
members of this genus sampled with Eurasian/Madagascar intra-specifi c variation, while divergences of 7.5% or greater
distributions, and excluding the African species S. remyi are present at the inter-specifi c level (see also Ruedi et al.,
and S. varilla. Within the Asian clade, two groups were 1998; Meegaskumbura & Schneider, 2008). Although relying
resolved, corresponding to the pygmy and the larger Suncus on a genetic species concept based solely on mitochondrial
species. The monophyletic pygmy shrew clade contained DNA to classify samples of uncertain taxonomic rank can
S. madagascariensis, S. etruscus and S. malayanus and be problematic (Ferguson, 2002), this approach is still useful
was well supported, with a BA posterior probability of 1.0 when the morphology of the taxa being compared is quite
and 100% bootstrap support in the NJ analysis. Within this conserved, as is the case in pygmy shrews.
clade, the monophyly of S. malayanus was well supported.
Both analyses indicated that S. etruscus is paraphyletic, The notably low “inter-specific” divergence of 1.4%
with the Sri Lankan S. etruscus consistently sister to S. between S. madagascariensis and Sri Lankan S. etruscus
madagascariensis, refl ecting the low divergence observed was significantly less than the intra-specific divergence
between these populations in pairwise estimates. present among the most distinct S. etruscus individuals
(up to 3.6% K2P distance; Table 2). This indicates that S.
madagascariensis, that is treated as endemic to Madagascar
DISCUSSION (Hutterer, 2005), and S. etruscus should not be considered
separate species and that the former is a junior synonym
The phylogenetic reconstruction presented here demonstrates of the latter. Furthermore, animals originally identifi ed as
that pygmy shrews from Italy, France, Sri Lanka, Madagascar S. madagascariensis are more closely related to Asian S.
and Malaysia form a monophyletic clade to the exclusion etruscus than those from Europe.
of other Asian and African shrews of the genus Suncus.
Although the taxon sampling in southeastern Asia is still We hypothesize that the Madagascar population recently
incomplete, we confi rm that the morphological resemblance colonized the island with founding animals originating from
among Eurasian taxa included in the S. etruscus species the Indian Subcontinent or Southeast Asia, presumably
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THE RAFFLES BULLETIN OF ZOOLOGY 2011
Fig. 2. The neighbour-joining (A) and Bayesian (B) trees for Suncus inferred from 1140 base-pairs of cytochrome b gene sequence. Bootstrap
and posterior probability values are given above branches.
241
Omar et al.: Phylogenetic relationships of pygmy shrews
transported by maritime travellers. The earliest evidence that historically, elevation has been an important factor in
of humans on Madagascar is slightly more than 2,000 limiting gene fl ow among S. malayanus populations in this
years ago and during the 11th–14th centuries there was region. More geographically extensive sampling across the
extensive maritime movement between portions of Asia and Thai-Malay peninsula will be necessary to ascertain whether
Madagascar (Burney et al., 2004). This situation is similar either of these hypotheses is true for S. malayanus and
to that of the large, commensal musk shrew (S. murinus), to unravel its northern and western range limits. Further,
where all African and Malagasy populations are considered as samples from northern and central Thailand also need to
recent introductions due to human trade (Hutterer & Tranier, be included in subsequent studies to investigate the level of
1990). Unlike the relatively robust musk shrew, however, divergence between S. malayanus and the endemic Borneo
S. etruscus is a notably small species, but given its broad pygmy shrew S. hosei.
geographical range, it appears to be adapted to a wide range
of environmental conditions (see below), and might have In conclusion, this study demonstrates that S. malayanus,
survived translocation in, for example, soil associated with which is endemic to the Thai-Malay peninsula, represents a
the shipment of live commercial plants (tea or coffee) or in unique lineage among Suncus pygmy shrews distinct from
boat holds containing invertebrate populations. Elsewhere, the S. etruscus species complex. It also provides information
in the Mediterranean region, S. etruscus is also believed to on the extent of genetic variation present among S. etruscus
have reached remote islands though passive human transport individuals, and shows that animals previously considered
(Dobson, 1998). Another potential species of pygmy shrew, S. madagascariensis are taxonomically synonymous
S. coquereli, is named from Mayotte in the Comores with S. etruscus. The Malagasy animals were most likely
Archipelago in close proximity to Madagascar. Although introduced to Madagascar via human intervention from a
we lack tissue samples of this population, Hutterer (2005) Indian Subcontinent or Southeast Asia source population.
indicated that close genetic similarity exists between this For a better understanding of the evolutionary history of
taxon and Malagasy individuals. We strongly suspect that different forms in the etruscus group, other taxa recognised
its status is similar to S. “madagascariensis” and therefore, by Hutterer (2005) as distinct species, notably S. hosei and
that S. coquereli actually represents another introduced form S. fellowesgordoni, also need to be included in subsequent
of S. etruscus. studies to investigate their level of genetic divergence.
In contrast, the level of genetic divergence present between S.
malayanus and the other Eurasian pygmy shrews (6.1–8.5%) ACKNOWLEDGEMENTS
suggests that Malayan populations have been evolving
We would like to thank the Wildlife and National Parks
independently for a relatively long period and are best
considered as a distinct species. In addition, S. malayanus is Department, Malaysia for permits to collect specimens; the
Forestry Department, Malaysia, for permits to work in forest
ecologically different from its European relative, as it lives
reserves; staff members of the Institute of Biological Sciences
in tropical humid forests, including montane habitats (see
and Ulu Gombak Field Studies Centre, University of Malaya,
Fig. 1 and trapping sites in Materials & Method section),
for assistance in the laboratory or during fi eld work; Prof. Dr.
whereas Eurasian S. etruscus is adapted to much more xeric
Shukor bin Md Nor, Universiti Kebangsaan Malaysia, for the
and lowland habitats (Spitzenberger, 1990). The Malagasy
sample from Bukit Rengit; and Dr Mohammed Rizman bin
population of S. etruscus occurs in different biomes on
Idid, Bioinformatics and Computational Biology, University
Madagascar, ranging from notably dry habitats to tropical
of Malaya, for advice on sequence analysis. We are grateful
humid forests across an elevational gradient from near sea
to the Direction du Système des Aires Protégées, Direction
level to 1200 m (Soarimalala & Goodman, 2011). Hutterer
Générale de l’Environnement et des Forêts of Madagascar
(2005) mentioned possible morphologic differences between
for issuing permits to conduct faunal surveys. This study
S. malayanus and S. etruscus, but besides darker pelage
was partially supported by a Postgraduate Research Fund
coloration in the former (Fig. 1), we did not investigate this
from the University of Malaya (Account No.: PS124-
aspect further.
2008A and PS331-2009A). EAS Adamson also would like
to acknowledge the support of an Australian Government
The three S. malayanus individuals used in this study were
Endeavour Foundation Postdoctoral Research Fellowship. We
collected from three different localities within Peninsular
thank two anonymous reviewers for their useful comments
Malaysia. The Cameron Highlands site is situated at an
on a previous version of the manuscript.
elevation of about 1465 m, while the other two locations
(Bukit Rengit and Ulu Gombak) are at lower elevations
(<500 m) and within about 65 km distance from one another.
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